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Signatures of adaptation in the weedy rice genome

Abstract

Crop domestication provided the calories that fueled the rise of civilization1,2,3. For many crop species, domestication was accompanied by the evolution of weedy crop relatives, which aggressively outcompete crops and reduce harvests4,5,6. Understanding the genetic mechanisms that underlie the evolution of weedy crop relatives is critical for agricultural weed management and food security. Here we use whole-genome sequences to examine the origin and adaptation of the two major strains of weedy rice found in the United States. We find that de-domestication from cultivated ancestors has had a major role in their evolution, with relatively few genetic changes required for the emergence of weediness traits. Weed strains likely evolved both early and late in the history of rice cultivation and represent an under-recognized component of the domestication process. Genomic regions identified here that show evidence of selection can be considered candidates for future genetic and functional analyses for rice improvement.

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Figure 1: Neighbor-joining tree of the 183 wild, cultivated, and weedy rice accessions.
Figure 2: Origin models for SH, BHA, and Chinese weedy rice.
Figure 3: Candidate genomic regions under selection in weedy rice.
Figure 4: Selective sweeps in the weedy rice genome.

Accession codes

Primary accessions

Sequence Read Archive

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Acknowledgements

We thank M. Dyer and staff of the University greenhouse for assistance in growing plants and L. Small for technical laboratory assistance. We are grateful to members of the Olsen laboratory for helpful comments on this manuscript. This work is supported by the National Science Foundation Plant Genome Research Program (IOS-1032023). The USDA is an equal opportunity provider and employer.

Author information

Authors and Affiliations

Authors

Contributions

K.M.O., Y.J. and A.L.C. designed the experiments. L.-F.L. and Y.-L.L. analyzed the data. L.-F.L., K.M.O. and A.L.C. wrote the manuscript.

Corresponding authors

Correspondence to Ana L Caicedo or Kenneth M Olsen.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Neighbor-joining tree of the 183 wild, cultivated, and weedy rice accessions.

Relationships of cultivated and wild rice correspond to previously observed relationships40. Wild rice accessions (dark green) are divided into different groups. The japonica (orange) and aromatic (light green) rice varieties form a clade. The BHA (red), SH (purple), and Chinese (black) weedy rice strains cluster with indica (light blue) and aus (pink), respectively. Bootstrap values (>50) are shown on each branch.

Supplementary Figure 2 Ancestral population structures of 183 rice accessions.

(a,b) Analyses of the full data set (a) and no-missing data set (b) were performed separately. Each vertical bar represents one accession, and different colors indicate distinct ancestry states. Cross-validation error was estimated for diverse K values from two to five. K = 3 minimizes the cross-validation error.

Supplementary Figure 3 Distributions of wild- and crop-specific private SNPs in SH (orange), BHA (red), and Chinese (green) weedy rice at the whole-genome level.

The box corresponds to the 95% confidence interval, and the black bar within each box is the mean value. The blue horizontal dashed line represents the equal proportion of wild- and crop-specific private SNPs. Positive and negative values represent crop-like and wild-like, respectively.

Supplementary Figure 4 Distribution patterns of wild- and crop-specific private SNPs within each chromosome of SH (orange), BHA (red), and Chinese (green) weedy rice.

The box corresponds to the 95% confidence interval, and the black bar within each box is the mean value for each chromosome. The blue horizontal dotted line represents zero. Positive and negative values represent the presence of crop-like and wild-like SNPs, respectively.

Supplementary Figure 5 Decrease in nucleotide diversity (θ) in SH and BHA weedy rice as compared to their crop ancestors.

The y axis represents the ratio of nucleotide diversity (θ) between weedy rice and their crop ancestors. Each bar is a 100-kb window, and the red solid line corresponds to the threshold for the top 5%. The numbers on the red line are the exact thresholds for each comparison.

Supplementary Figure 6 Gene Ontology (GO) analysis of the 178 candidate genes in SH weedy rice.

Supplementary Figure 7 Gene Ontology (GO) analysis of the 307 candidate genes in BHA weedy rice.

Supplementary Figure 8 Ratio of nucleotide diversity (π) between indica and SH weedy rice across the genome.

(a) The criteria MQ ≥ 10 and DP ≥ 1 were used to filter the reported variants. (b) The criteria MQ ≥ 20 and DP ≥ 3 were used to filter the reported variants. (c) The criteria MQ ≥ 10 and DP ≥ 1 were used, excluding low-frequency (<2%) heterozygosity. Each bar represents a 100-kb window.

Supplementary Figure 9 Genome-wide genetic differentiation (FST) between indica and SH weedy rice across the genome.

(a) The criteria MQ ≥ 10 and DP ≥ 1 were used to filter the reported variants. (b) The criteria MQ ≥ 20 and DP ≥ 3 were used to filter the reported variants. (c) The criteria MQ ≥ 10 and DP ≥ 1 were used, excluding low-frequency (<2%) heterozygosity. Each bar represents a 100-kb window.

Supplementary Figure 10 Ratio of nucleotide diversity (π) between BHA and aus across the genome.

(a) The criteria MQ ≥ 10 and DP ≥ 1 were used to filter the reported variants. (b) The criteria MQ ≥ 20 and DP ≥ 3 were used to filter the reported variants. (c) The criteria MQ ≥ 10 and DP ≥ 1 were used, excluding low-frequency (<2%) heterozygosity. Each bar represents a 100-kb window.

Supplementary Figure 11 Genome-wide genetic differentiation (FST) between BHA and aus across the genome.

(a) The criteria MQ ≥ 10 and DP ≥ 1 were used to filter the reported variants. (b) The criteria MQ ≥ 20 and DP ≥ 3 were used to filter the reported variants. (c) The criteria MQ ≥ 10 and DP ≥ 1 were used, excluding low-frequency (<2%) heterozygosity. Each bar represents a 100-kb window.

Supplementary Figure 12 Ratio of nucleotide diversity (π) between wild and cultivated rice across the genome.

(a) The criteria MQ ≥ 10 and DP ≥ 1 were used to filter the reported variants. (b) The criteria MQ ≥ 20 and DP ≥ 3 were used to filter the reported variants. (c) The criteria MQ ≥ 10 and DP ≥ 1 were used, excluding low-frequency (<2%) heterozygosity. Each bar represents a 100-kb window.

Supplementary Figure 13 Genome-wide genetic differentiation (FST) between wild and cultivated rice across the genome.

(a) The criteria MQ ≥ 10 and DP ≥ 1 were used to filter the reported variants. (b) The criteria MQ ≥ 20 and DP ≥ 3 were used to filter the reported variants. (c) The criteria MQ ≥ 10 and DP ≥ 1 were used, excluding low-frequency (<2%) heterozygosity. Each bar represents a 100-kb window.

Supplementary Figure 14 Ratio of nucleotide diversity (π) between wild and cultivated rice.

The identified domestication genes are shown for each chromosome.

Supplementary Figure 15 Ratio of nucleotide diversities (θ and π) between wild, cultivated, and weedy rice.

The y and x axes are the ratio of θ and π, respectively.

Supplementary Figure 16 Neighbor-joining tree based on the 54 selected rice accessions.

Relationships of cultivated and wild rice correspond to previously observed relationships40. Wild rice accessions (dark green) are divided into different groups. The japonica (orange) and aromatic (light green) rice varieties form a clade. The BHA (red), SH (purple), and Chinese (black) weedy rice strains cluster with indica (light blue) and aus (pink), respectively. Bootstrap values (>50) are shown on each branch.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–16 and Supplementary Tables 2, 4–6 and 14 (PDF 2846 kb)

Supplementary Table 1

The list of 183 accessions of wild, cultivated, and weedy rice species sampled in the collection. (XLSX 59 kb)

Supplementary Table 3

Genetic assignments at wild, cultivated, and weedy rice accessions from two to five. (XLSX 59 kb)

Supplementary Table 7

Causative mutations of domestication genes in the three types of weedy rice. (XLSX 37 kb)

Supplementary Table 8

Genome-wide detection of regions of low nucleotide diversity in SH compared to indica. (XLSX 52 kb)

Supplementary Table 9

Genome-wide detection of regions of low nucleotide diversity in BHA compared to aus. (XLSX 53 kb)

Supplementary Table 10

Functionally characterized genes showing low nucleotide diversity in SH and high genetic differentiation between SH and indica. (XLSX 57 kb)

Supplementary Table 11

Functionally characterized genes showing low nucleotide diversity in BHA and high genetic differentiation between BHA and aus. (XLSX 70 kb)

Supplementary Table 12

Number of raw variants in wild, cultivated, and weedy rice with different filter criteria. (XLSX 42 kb)

Supplementary Table 13

Genome-wide detection and functional annotation of selective sweep regions in the full crop populations. (XLSX 54 kb)

Supplementary Data

Sequence alignment of Rc genes in wild, cultivated, and weedy rice. (TXT 2000 kb)

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Li, LF., Li, YL., Jia, Y. et al. Signatures of adaptation in the weedy rice genome. Nat Genet 49, 811–814 (2017). https://doi.org/10.1038/ng.3825

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